The role of compensatory movements patterns in spontaneous recovery after stroke.

[Purpose] Post-stroke motor recovery consists of both true recovery and compensatory movements. Although compensatory movements are learned more quickly early after stroke, the role of compensatory movement patterns in functional recovery is controversial. We investigated the role of compensatory movement patterns in the long-term functional motor recovery after stroke.
[Subjects and Methods] Male Wistar rats were subjected to photothrombotic infarction to induce motor and sensorimotor cortex lesions. The rats were given task-specific training. Behavior tests and analyses of compensatory movement patterns (head lift, limb withdrawal impairment, phantom grasps, and pellet chasing) during the single-pellet reaching test were performed 2, 7, 14, 21, 28, and 35 days post stroke.
[Results] Successful retrieval during the single-pellet reaching test was significantly correlated with compensatory movement patterns in stroke groups. Motor cortex stroke showed significant correlation in limb withdrawal impairment and pellet chasing. But, sensorimotor cortex stroke was significant correlation in pellet chasing.
[Conclusion] The data suggest that compensatory movements after stroke are correlated with spontaneous recovery. Since some compensatory movement patterns are detrimental to functional recovery, the correct timing of training and control of compensatory movement patterns might be important.

INTRODUCTION

Compensatory movement is frequently observed in stroke patients, and accompanies poor functional outcomes. Therefore, it is useful to elucidate the factors contributing to compensatory movement because it would allow us to develop preventive or therapeutic strategies1). Animals might compensate for an impairment by substituting a new behavior to achieve a previous goal, or they might display true recovery in which they regain a pre-stroke behavior2). In compensation, a new behavior is substituted for a lost behavior, whereas in recovery, the original behavior is restored. Distinguishing between these processes is important because: (1) compensation can be mistaken for recovery; (2) compensatory strategies can disrupt performance; (3) the behavioral methods, therapy, and neural changes associated with enhancing compensation can differ from those associated with recovery; and (4) under different conditions both compensation and recovery may be desirable outcomes3). Post-stroke behavioral change is important, but the contribution of each of these factors to compensation versus recovery is not fully understood. Therefore, we examined the relationship between recovery and compensatory movement patterns (CMPs) and discussed the role of CMPs in the long-term post-stroke functional recovery. To determine the role of CMPs in motor recovery after stroke, we investigated the role of CMPs in the long-term functional recovery after stroke.

SUBJECTS AND METHODS

Twelve 8-week-old male Wistar rats (Orient Bio Experimental Animal Center, Seongnam, Gyeonggi-do, Korea) weighing 250–300 g were used in this study. The rats were housed in colony cages and maintained with a 12-h light/dark cycle, with free access to food and water. All procedures were approved by the Animal Experiment Review Board of the Laboratory Animal Research Center of Konkuk University (Approval no. KU14151).

Rats were assigned randomly to one of three experimental groups: (1) the sham control (SC) (n=4), (2) motor cortex (MC) stroke (n=4), and (3) sensorimotor cortex (SMC) stroke (n=4) groups. Focal cortical infarcts were produced by focusing light on the sensorimotor and motor cortexes in Rose Bengal-treated rats. Briefly, the rats were anesthetized with a mixture of ketamine and Rompun (30 mg/kg, i.p.), placed in a stereotaxic frame, and the skull was exposed. A cold white light with 4 m and 2 m apertures was positioned over the bregma and 4.0 mm lateral to the midline over the sensorimotor and motor cortexes. The photochemical dye Rose Bengal (Sigma-Aldrich) was dissolved in 0.9% NaCl at a dose of 10 mg/kg and infused into the femoral veins of the rats in the two experimental groups via a micro-injection pump within 5 minutes. Then, the light was turned on for 20 min4). The reaching behavior success was measured using a single-pellet reaching test (SPRT). A successful reach was defined as one in which an animal grasped a food pellet, brought it into the cage using its paw, and placed it in its mouth. Success (%) was the number of pellets obtained/total number of trials × 100. First-trial successes were trials in which a rat obtained a food pellet on the first advance of the limb toward the food5). Compensatory movement patterns (CMPs) were counted during the total number of trials of the SPRT. Both experimental groups had impaired lifting and aiming components of reach and in supination of the paw upon withdrawal and in releasing the food into the mouth. The effects of the motor and sensorimotor cortex lesions on reaching behavior were described, including the effects of variation in lesion size on behavior, and the effects of treatments designed to minimize post-lesion impairments. The animals were filmed in frontal and ventral views 1 day before and 2, 7, 14, 21, 28, and 35 days after photothrombotic ischemia with a Sony HDR-CX350 Handycam. The tapes were viewed on a Sony DV cam HDR-CX350 player. Representative movements were captured using GOM Player ver. 2.2 software on a Windows 7 computer. The SPRT was analyzed using one-way repeated measures analysis of variance (ANOVA), followed by a post hoc Newman-Keuls multiple comparisons test. The correlation of CMPs with a successful SPRT was analyzed using Pearson’s correlation coefficient. All data are expressed as the mean ± standard deviation. The null hypothesis that there was no difference was rejected if p < 0.05. All data analyses were performed using SPSS ver. 22.0.

RESULTS

We examined the effects of spontaneous recovery after stroke using a single-pellet reaching test. The reaching success was measured as the number of pellets retrieved and eaten on the side contralateral to the lesion, expressed as the percentage of 20 trials in which a pellet was obtained. There were significant effects of group (F3,13 = 6.03; p < 0.01) and time (F6,78 = 21.00; p < 0.001), and a significant interaction of group × time (F18,78 = 3.62; p < 0.001). The reaching ability was assessed 2 days and 1, 2, 3, 4, and 5 weeks after stroke. The MC stroke group showed profoundly impaired reaching success 2 days and 1 week after the stroke. The SMC stroke group showed profoundly impaired reaching success 2 days and 1, 2, 3, 4, and 5 weeks after the stroke. There were significant effects of group (F4,35 = 36.84; p < 0.001) and time (F6,210 = 91.76; p < 0.001), and a significant interaction of group × time (F24,210 = 9.34; p < 0.001). The SMC stroke group showed improved reaching ability beginning 3 weeks after stroke compared with the MC stroke group.

Although the component scores of the MC and SMC stroke groups were similar, inspection of the rats’ movements suggested that the respective group scores originated in part from different sources, as indicated by differences in head lifts, limb withdrawal impairment, and pellet chasing. The large stroke group used more body rotation to center the limb on the slot and they raised their head and forequarters, presumably to assist in lifting the reaching limb to the level of the shelf. They showed impaired limb withdrawal and typically lifted and partially supinated the paw before withdrawing it from the slot. Once the paw was removed from the slot, it was supinated and the digits were opened to release the food pellet into the mouth. Both the MC and SMC stroke rats showed impaired supination of the paw, so they turned their snouts toward the paw. The limb withdrawal impairment, pellet chasing, phantom grasps, and head lifts were observed in the SMC stroke group on all postsurgical days (Table 1). The improvement is attributed to compensatory strategies, such as substituting trunk rotation for the lost rotatory movement of the forelimb, which occurred during transport and withdrawal in MC stroke group. The sensorimotor cortical stroke group showed an increase in the success rate of the SPRT that was accompanied by increased CMPs, particularly including pellet chasing (p < 0.05). The success rate of spontaneous recovery was increased through CMPs. The MC stroke group showed a significant correlation between CMPs and the success rate of SPRT with limb withdrawal impairment and pellet chasing (p < 0.05).

Table 1.

Correlations with the success rate of the SPRT in MC and SMC stroke

	MC stroke (n=4)	SMC stroke (n=6)
	r	r
Limb withdrawal impairment	–0.668**	0.738
Pellet chasing	–0.705**	0.827*
Phantom grasps	–	0.718
Head lifts	–	0.585

** p< 0.05 and ** p < 0.001 vs. successful retrievals

DISCUSSION

Our data suggest that compensatory movement patterns after stroke depend on stroke severity. CMPs are involved in the post-stroke spontaneous recovery of motor function. CMPs might act by either disrupting or enhancing performance of a task. CMPs might be involved in the timing of rehabilitation and affect functional recovery. Friel and Nudo6) examined the CMPs during behavioral recovery after an experimental cortical injury in non-human primates. Observations of behavioral recovery might be important for future studies. The animals showed various CMPs7). For recovery, CMPs as abnormal patterns in acute hemiparesis should be suppressed6). Treatment methods such as neuromuscular development treatment, constraint-induced movement therapy, and task-oriented training focus on avoiding the learned disuse of the paretic upper limb and using it with minimal compensatory movement patterns8, 9). The underlying cause of the functional recovery might be very important for both the optimal timing of rehabilitation and regulating compensatory movement patterns. Substantial functional recovery might occur via the use of CMPs.